Patterns in Ericaceae: New Phylogenetic Analyses

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BS 55 479 Origins and biogeographic patterns in Ericaceae: New insights from recent phylogenetic analyses

Kathleen A. Kron and James L. Luteyn

Kron, KA. & Luteyn, J.L. 2005. Origins and biogeographic patterns in Ericaceae: New insights from recent phylogenetic analyses. Biol. Skr. 55: 479-500. ISSN 0366-3612. ISBN 87-7304-304-4.

Ericaceae are a diverse group of woody plants that span the temperate and tropical regions of the world. Previous workers have suggested that Ericaceae originated in Gondwana, but recent phy logenetic studies do not support this idea. The theory of a Gondwanan origin for the group was based on the concentration of species richness in the Andes, southern Africa, and the southwest Pacific islands (most of which are thought to be of Gondwanan origin). The Andean diversity is comprised primarily of Vaccinieae with more than 800 species occurring in northern South America, Central America, and the Antilles. In the Cape Region of South Africa the genus Erica is highly diverse with over 600 species currently recognized. In the southwest Pacific islands, Vac cinieae and Rhodoreae are very diverse with over 290 species of Rhododendron (sect. Vireya) and approximately 500 species of Vaccinieae (I)imorphanthera, Paphia, Vaccinium). Recent phyloge netic studies have also shown that the Styphelioideae (formerly Epacridaceae) are included within Ericaceae, thus adding a fourth extremely diverse group (approximately 520 species) in areas considered Gondwanan in origin. Phylogenetic studies of the family on a global scale, how ever, have indicated that these highly diverse “Gondwanan” groups are actually derived from within Ericaceae. Both Fitch parsimony character optimization (using MacClade 4.0) and dispersal-vicariance analysis (DIVA) indicate that Ericaceae is Laurasian in origin. Thus, previous sug gestions that Ericaceae are Gondwanan in origin are not supported. Separate analysis of geo graphic areas and phylogenetic relationships among the diverse South American Vaccinieae using dispersal-vicariance analysis (DIVA) indicate that dispersal has likely played a major role in the diversification of the Andean clade of Vaccinieae into Central America and the lower eleva tions in northern South America. Results of the analysis indicate an Andean origin for this group, which comprises most of the ericaceous species diversity described from South America. This analysis also indicates that in taxa such as Cavendishia and Satyria s.s., the Central American species are the result of relatively recent dispersal from a South American (i.e., Andean) ancestor.

Kathleen A. Kron, Department of Biology, Wake Forest University, Winston-Salem, North Carolina, 27109- 7325, U.S.A. E-mail: [email protected]

James L. Luteyn, New York Botanical Garden, Bronx, New York, 10458-5126, U.S.A. E-mail: jluteyn@nybg. org 480 BS 55

Introduction regions of the world. These concentrations of diversity occur in four major clades within Eri Ecologically and economically important, the caceae: Vaccinieae, Rhodoreae, Ericeae, and Ericaceae are a diverse group of woody plants Styphelioideae (Appendix 1). Vaccinieae are that can be found in a variety of habitats most diverse in the montane tropics of South throughout much of the temperate and tropi America and Asia. Although generic limits cal regions of the world (Appendix 1). They within Vaccinieae are poorly understood, phy are usually found in acid soils and are associ logenetic studies have shown that of the five ated with mycorrhizal fungi. In the tropics, Eri major clades identified in a molecular system caceae are most diverse in mid- to high-eleva atic study of the group (Kron et al. 2002b), tion montane cloud forests (Luteyn 2002), those with the largest number of species are which are also some of the most threatened tropical and occur in Gondwanan regions (e.g., ecosystems in the world (Knapp 2002). The South America, New Guinea). In the Rhodor most recent classification of the family (Kron et eae, Rhododendron section Vireya is the most al. 2002a) recognizes eight subfamilies and 20 species rich group within Rhododendron. Vireyas tribes. The distribution of these groups is gen are tropical and most diverse in New Guinea. erally cosmopolitan in scale, with concentra Africa, another Gondwanan region, also has tions of species diversity in the tropics, the large and morphologically diverse Erica Himalayas, Australia, and the Cape Region of (Ericeae) and one of the highest concentra South Africa (Fig. 1, Appendix 1). tions of species in a single genus in the world in The most recent global treatment of Eri the Cape Region. Lastly, Styphelioideae, which caceae biogeography is by Raven and Axelrod contain approximately 450 species are most (1974) who presented a general overview of diverse in Australia. This group was formerly the biogeography of angiosperms and sug thought to be distinct from Ericaceae, but gested that Ericaceae (not including Styphe- recent phylogenetic studies using molecular lioideae, then a separate family, Epacridaceae) and morphological data have shown that the likely originated in Gondwana with direct group is sister to the Vaccinioideae (Kron et al. migration from Africa to South America. They 2002a) and therefore derived from within Eri considered that long distance dispersal from caceae. North America in the late Miocene had added Recent phylogenetic analyses in Ericaceae to the diversity of Ericaceae in South America, have provided good resolution with strong sta which was already established there via the ear tistical support of major clades within the fam lier African-South American land connection. ily based on both molecular and morphologi The Styphelioideae (Epacridaceae) were con cal data. With this phylogenetic framework, sidered to be of relatively ancient descent biogeographic patterns may be analyzed with resulting from long distance dispersal between the goal of shedding some light on the origins west Gondwana and Australasia (Raven & Axel of the group. Here we investigate the origin rod 1974). Heads (2003) postulated a globally and biogeographic patterns of Ericaceae using widespread complex as ancestral to Ericaceae, dispersal-vicariance analysis (DIVA; Ronquist but his supporting argument was confined to 1997) and Fitch parsimony character optimiza descriptions of Malesian ericad distributions. tion using MacClade 4.0 (Maddison & Maddi- The most species-rich groups within the Eri son 2000). In addition, the biogeographic caceae do indeed appear to be concentrated in areas of the Andean clade within the Vac what are now considered to be Gondwanan cinieae are analyzed using DIVA. BS 55 481

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Methods morphological (91 characters) data for the Eri caceae tree. The sampling of ericalean taxa is In addition to DIVA and Fitch parsimony char relatively small, but relationships in the tree acter optimization, there are several other are in general agreement with the recent study approaches to biogeographic analysis (c.g., by Anderberg et al. (2002) that used more COMPONENT; Page 1993,). We chose DIVA genes and many more taxa. For the Andean because it can be used with a single phyloge clade analysis we used the most recent molecu netic tree, rather than requiring trees from sev lar tree based on three chloroplast eral different groups in order to construct area genes/regions (matK, ndhF, rps4) and the cladograms. DIVA does not require any a prior nuclear internal transcribed spacer region, ITS knowledge of geologic history and does not (Powell 8c Kron 2003). All of the trees used for assume areas have a strictly divergent history biogeographic analysis exhibited moderate to (Ronquist 1997). DIVA treats areas as charac strong bootstrap support for most clades. Few ters (in a presence/absence format), but mini polytomies were present in the Ericales and mizes dispersal and extinction events relative Andean trees, and the Ericaceae tree was fully to vicariance (no cost) events in ancestral state resolved. Because DIVA requires fully resolved (?>., area) reconstruction. Therefore, DIVA trees, the Ericales tree of Kron et al. (2002a) offers the possibility of identifying potential was resolved according to the results of more vicariance events at deep branches in the tree. detailed analyses (Kron et al. 2002a; Kron However, the deepest nodes within the tree are 1997) and the Andean tree was resolved arbi also prone to more error (Ronquist 1997), so it trarily. The Ericales tree was modified to is important to evaluate the group of interest at include an additional taxon (i.e., Clethra more than one taxonomic scale. arborea, authors of species names are given in Fitch parsimony character optimization uses Appendices 2-4) in order to better represent areas as character states and these are mapped the geographic distribution of the Clethraceae. onto the tree using MacClade 4.0 (Maddison & The placement of C. arborea sister to C. alnifolia Maddison 2000). This provides a simple way of was based on the analysis of Anderberg et al. viewing the distribution of current taxa relative (2002) which provided better statistical sup to the branching patterns in the tree. However, port and resolution for nodes basal to the Eri Fitch parsimony optimization allows fewer pos caceae. Two widespread species were removed sible ancestral area reconstructions than DIVA from the Andean clade to facilitate the DIVA because only terminals can have more than analysis. one state (i.e., area). In the biogeographic analysis of Ericaceae We investigated the origin of Ericaceae using (both the Ericales tree and the Ericaceae two trees. One tree included Ericaceae and sev tree) different scorings of areas for DIVA and eral other members of the Ericales (APG 1998) Fitch parsimony character optimization were and the other tree included more taxa within used. The broadest scoring (largest scale) Ericaceae, but was rooted with Enkianthus. Phy used geologic information and present day logenetic trees for Ericaceae, and for the sub distribution to define a Laurasian area and a set of the Ericales were obtained from pub Gondwanan area. The designation of a pre lished results in Kron et al. (2002a). These trees sent day location as Laurasian or Gondwanan were obtained using molecular data {matK, was determined by geologic reconstructions rbcL, nr 18s) for the Ericales tree, and com that place current regions in previously exist bined analysis of molecular (matK, rbcL) and ing supercontinents (c.g., Hallam 1994; BS 55 483

Scotese 2000). A smaller scale designation of North American + Eurasian origin for Eri areas used present day distributions on exist caceae. In the Ericales tree, both Fitch charac ing continents as areas. In the Andean clade ter optimization and DIVA failed to result in analysis, five areas were recognized: Central definitive ancestral areas for some of the America, Chocô (NW Colombian lowlands), deeper branches within Ericaceae. DIVA iden Andean highland arc, an eastern lowland arc, tified several equally optimal reconstructions and the Antilles. at the Arbutus canariensis to Vaccinium macrocar- Terminals in the biogeographic analyses are pon node, as well as the next two nodes lead species, the same terminals as those in the mol ing to the rest of the Ericaceae. Fitch analysis ecular and molecular plus morphological phy using more taxa within Ericaceae (Fig. 5) indi logenetic analyses used to obtain the trees cated North America as an ancestral area for (Kron et al. 2002a; Powell & Kron in press). many clades within the family, but was equivo Although using species as terminals may not cal in its assessment of ancestral areas at the include the entire geographic range of the base of the tree. DIVA assigned North America clade of interest, it avoids the same problems and Asia or North America, Asia, and Europe encountered when using higher taxa as termi as the Most Recent Common Area (MRCA) in nals in cladistic analyses, such as polymor two of the three equally optimal reconstruc phisms and potential lack of monophyly (Kron tions of ancestral areas at the base of the Eri &Judd 1997; Ronquist 1997; Wiens 1998). caceae tree (Fig. 6). A third equally optimal For each analysis a matrix was constructed ancestral reconstruction is Africa + North in MacClade 4.0. Matrices constructed for the America, Asia, and Europe. However, in DIVA DIVA analyses used areas as characters and the reliability of ancestral assignments scored taxa as present or absent for each area decreases deeper in the tree (Ronquist 1997). (Appendices 2-4). These matrices were then Taking this into consideration along with the converted to batch files and analyzed using fact that the first two optimized areas in the the DIVA software instructions outlined in Ericaceae tree correspond to the results of the Ronquist (1997). The “printrecs” command DIVA analysis of Ericales, these results clearly was used to find all of the equally optimal indicate a Laurasian origin for Ericaceae. reconstructions. Fitch parsimony character Within the Ericaceae, Fitch parsimony charac optimization was performed in MacClade 4.0 ter optimization (Fig. 5) indicates North using the trees obtained from Kron et al. America as the ancestral area for much of the (2002a) and Powell and Kron (2003). Matri group. DIVA analysis (Fig. 6) indicates North ces constructed for these analyses (Appen America as a key ancestral area for the origin dices 2 and 3) designated areas as alternate of Vaccinioideae and Ericoideae. Within Vac- states of a single character (z.c., geographic cinioideae DIVA analysis indicates that there distribution). have been at least two dispersals into South America leading to the Vaccinieae and por tions of Gaultherieae (Fig. 6). Ancestral area Results reconstruction within Gaultherieae is not Both Fitch parsimony character optimization clear, with DIVA recognizing several equally and DIVA analyses indicate a Laurasian origin optimal ancestral areas at the Gaultheria-Diply- for Ericaceae (Figs. 2, 3). DIVA analysis of the cosia-Tepuia node (Fig. 6). Within the Styphe- Ericalean matrix using smaller scale areas lioideae the occurrence of Lebetanthus (Fig. 4) indicated either a North American, or myrsinites, endemic to southern Ghile, is indi- 484 ERICACEAE _j -J — — _l — — — _j _J — _l — — 0 0 0 0 0 0 0 J J 1 I I I I 1

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cated as a dispersal event. North America is before any detailed conclusions can be made also indicated as the MRCA of Ericoideae (Fig. about the role of dispersal in tropical blue 6). The presence of Bejaria and Ledothamnus in berry speciation. South America is indicated as the result of one or more dispersal events. Within the Rhodor- eae, several equally optimal reconstructions Discussion are indicated, but all of these suggest a The earliest published fossil evidence for likely Laurasian origin. Nevertheless, the Asian existence of Ericaceae based on flowers is Pale- diversification of Rhododendron (here repre oenkianthus (Nixon & Crepet 1993). This fossil sented by R. tsusiophyllum and R. kaempferï) was found in Turonian deposits in North appears to be relatively recent. The Ericeae + America (New Jersey) and, if correctly identi Empetreae clade has a MRCA of North Amer fied, indicates the existence of Ericaceae in the ica + Europe with a vicariance event indicated Late Cretaceous (~90 mya). At that time, pale in the divergence between Ericeae (Europe + ogeographic plate reconstructions (Cox 1974; Asia) and Empetreae (North America). How Scotese 2000) place eastern North America ever, these results are likely a simplification of connected to Europe (either directly or more complex biogeographic relationships through a series of islands) and northwestern because no representative of Empetrum (wide North America proximate, or possibly con spread in boreal latitudes, with disjunct E. nected, to Asia. The DIVA analyses (Figs. 3, 4, rubrum in southern South America) was 6) that indicate a Laurasian origin (either included in the analysis. The presence of Arb- North America, or North America + Eurasia) utoideae (represented by Arbutus canariensis for Ericaceae are therefore at least not in con and Arctostaphylos uva-ursi) in Africa is indi flict with the geological/tectonic information cated as a result of vicariance. The presently available. Based on at least some of Monotropoideae are generally widespread and the equally optimal reconstructions of ances DIVA indicates the MRCA of this clade as tral areas by DIVA, a widespread common North America + Europe. ancestor to the majority of Ericaceae (all Eri Analysis of biogeographic areas in the caceae but Enkianthus and Monotropoideae; Andean clade of the blueberry tribe (Vac- Fig. 3) may have occurred along the coastline cinieae) resulted in eight equally parsimonious of the developing Tethyan seaway and subse reconstructions (Fig. 7). DIVA indicates that quent vicariance may have been a major factor much of the diversification in Vaccinieae in the initial divergence of the ancestors of occurred in the Andean highland arc. More Arbutoideae, Ericoideae, and Vaccinioideae recent speciation may have been the result of due to the continued drifting apart of Africa, subsequent dispersal to lower elevations which Europe, and North America. Arbutoideae have could explain the distribution of Anthopterus been postulated as a group that diversified wardii and Satyria grandifolia in the Choco, and along the Tethys seaway (Hileman et al. 2001) Satyria cerander in French Guiana. The Thibau- which makes their occurrence in what is now dia clade is Andean in origin, as is the Cer- North America, Mediterranean Europe, Asia, atostema-Macleania clade. The results also indi and Africa comprehensible. However, clue to cate dispersal as the primary event responsible the lack of detailed phylogenetic studies of for the presence of Andean clade species in Arbutoideae, Ericoideae, and Vaccinioideae Central America. However, the sampling of these hypotheses remain to be tested. Vaccinieae must be much more complete The occurrence oflarge groups such as Erica BS 55 491 spp. and Styphelioideae in regions formerly groups most diverse in the tropics likely origi part of Gondwana is explained by dispersal nated there may be found in the boreotropics events according to DIVA. However, wide hypothesis. First put into a phylogenetic frame spread occurrence and subsequent extinction work by Lavin and Luckow (1993), the hypoth is an alternative that DIVA does not readily esis originally referred specifically to diversity indicate (Ronquist 1997). In the case of Sty- in tropical North America (Tiffney 1985a, b; phelioideae there is fossil evidence of the Wolfe 1975). The general pattern obtained occurrence of this group in southern Africa in from DIVA analysis of the Ericaceae is one that the Paleocene (Scholtz 1985) and in several supports a boreotropical origin for the group sites in northern Europe from the early with subsequently more recent diversification Eocene (~57 mya) to the late Miocene (~6.7 in tropical Asia, southern Africa, and tropical mya: data from The Paleobiology Database, South America. In addition, the results pre http: www.pbdb.org). DIVA analysis indicates a sented here support a North American origin widespread ancestor across Australia and for some of the major groups within Ericaceae North America at the Vaccinioideae-Styphe- such as Vaccinioideae and Ericoideae. Within lioideae node (Fig. 6), but these two areas were the Vaccinioideae, the MRCA of Gaultherieae never in direct contact. It seems more likely, (Kron et al. 2002b) is difficult to establish, as given the fossil evidence, that the ancestor to DIVA found seven equally optimal reconstruc Vaccinioideae and Styphelioideae was wide tions for this node (see double asterisk in Fig. spread and that vicariance and subsequent 6). The clarification of phylogenetic relation extinction of Styphelioideae in Europe and ships within Gaultherieae is obviously a prereq Africa are the causes of the present day distrib uisite for understanding the biogeographic his ution of Styphelioideae. Although the African tory of this clade. Gaultheria (including at least species of heather (Erica) were not included in Pernettya and possibly Diplycosia, see Powell & the analyses presented here, the addition of Kron 2001) is a complex group with the diver these taxa to the tree and subsequent DIVA sity of species concentrated in tropical Asia and analysis did not alter the hypothesis of disper around the Pacific rim. This is in contrast to sal from Eurasia to Africa (results not shown). most of the rest of the groups within Ericaceae This is because the African species of Erica are which tend to have a Laurasian pattern of dis monophyletic and derived from within the tribution. A more detailed knowledge of the European/W. Asian species of Erica (McGuire relationships among Gaultherieae would be 2003). Other African members of Ericaceae helpful in the analysis of its biogeographic his include species of Agarista and Vaccinium and, tory, but the present study would indicate that based on the results presented here, are likely dispersal is likely a major factor in the history to be attributed to long distance dispersal. of diversification of the clade, at least in the However, phylogenetic studies of these African case of species occurring in Tasmania and members of otherwise North American, Euro South America. Within the Ericoideae the pean, or Asian clades are necessary before common ancestral area for both the Rhodor- details of the biogeography of African Eri eae and Ericeae is North America. Ericeae is caceae can satisfactorily be addressed. In addi indicated as European in origin and the tion, other methods of biogeographic analysis African species by extension a more recent may provide more insight into the history of diversification. Ericaceae. The Andean clade represents a group of taxa An alternative to the general view that that contain many genera whose greatest 492 BS 55

species diversity occurs at higher elevations in Literature cited the Andes of northern South America. Inter estingly, this clade does not include any sam Anderberg, A.A., Rydin, C. & Källersjö, M. 2002. Phyloge pled species of Vhcczmttwz (Kron et al. 2002b) netic relationships in the order Ericales s.l.: analyses of molecular data from five genes from the plastid and and some genera such as Orthaea and Notopora mitochondrial genomes. Amer. J. Bot. 89: 677-687. also fall outside of the Andean clade. DIVA APG (Angiosperm Phylogeny Group). 1998. An ordinal analysis of the Andean clade indicates that the classification for the families of flowering plants. Ann. ancestor to the Andean + Mesoamerican- Missouri Bot. Gard. 85: 531-553. Caribbean clades may have been widespread in Cox, C.B. 1974. Vertebrate palaeodistributional patterns and continental drift./. Biogeogr. 1: 75-94. the Andes and the mountains of Central Amer Hallam, A. 1994. An Outline of Phanerozoic Biogeography. ica and the Antilles (Fig. 7). If this is the case, Oxford Biogeographic Series No. 10. Oxford University then the diversification within the Andean Press, New York. clade is very recent (since the late Miocene) Heads, M. 2003. Ericaceae in Malesia: vicariance, biogeog and the taxa that are currently found in Cen raphy, terrane tectonics, and ecology. Telopea 10: 311- 449. tral America (r.g., some species of Cavendishia Hileman, L.C., Vasey, M.C. & Parker, V.T. 2001. Phylogeny and Satyrià) are recent introductions via dis and biogeography of the Arbutoideae (Ericaceae): persal from the northern Andes. implications for the Madrean-Tethyan hypothesis. Syst. The biogeographic pattern (i.e., recent Bot. 26: 131-143. diversification in areas of Gondwanan origin) Knapp, S. 2002. Assessing patterns of plant endemism in neotropical uplands. Bot. Rev. (Lancaster) 68: 22-36. found in our analysis of the Andean clade of Kron, K.A. 1997. Phylogenetic relationships of Rhododen- Vaccinieae is representative of a more general droideae (Ericaceae). Amer. J. Bot. 84: 973-980. pattern found within Ericaceae. Based on cur Kron, K.A. & Judd, W.S. 1997. Systematics of the Lyonia rent phylogenetic studies (Kron et al. 2002a) group (Andromedeae, Ericaceae) and the use of species the occurrence in Gondwanan regions of as terminals in higher-level cladistic analyses. Syst. Bot. 22: 479-492. groups such as Rhododendron and Erica that Kron, K.A., Judd, W.S., Stevens, P.F., Crayn, D.M., Ander exhibit a wide range of morphological diversity berg, A.A., Gadek, P.A., Quinn, C.J. & Luteyn, J.L. 2002a. and large numbers of closely related species Phylogenetic classification of Ericaceae: molecular and are recent evolutionary phenomena rather morphological evidence. Bot. Rev. (Lancaster) 68: 335- than the result of ancient diversification. This 423. Kron, K.A., Powell, E.A. & Luteyn, J.L. 2002b. Phylogenetic is supported by the results of this study that relationships wihin the blueberry tribe (Vaccinieae, Eri indicate a Laurasian origin for the Ericaceae. caceae) based on sequence data from matK and nuclear ribosomal ITS regions, with comments on the placement of Satyria. Amer. J. Bot. 89: 327-336. Acknowledgements Lavin, M. & Luckow, M. 1993. Origins and relationships of tropical North America in the context of the boreotrop- We thank the following people and institu ics hypothesis. Amer. J. Bot. 80: 1-14. tions: W. S. Judd, S. Zona, A. A. Anderberg, C. Luteyn, J.L. 2002. Diversity, adaptation, and endemism in Gracie, P. Pedraza, K. Walter, J. L. Clark, T. neotropical Ericaceae: Biogeographical patterns in the Ness, P. Stevens, E. Brown, E. A. Powell, D. M. Vaccinieae. Bot. Rev. (Lancaster) 68: 55-87. Crayn, The National Science Foundation DEB Maddison, D.R. & Maddison, W.P. 2000. MacClade 4.0: Analysis of Phylogeny and Character Evolution. Version 4.0. 9628841, DEB 9407350, DEB 9903719, Wake Sinauer Associates, Sunderland, Massachusetts. Forest University, The New York Botanical Gar McGuire, A.F. 2003. Phylogeny and biogeography of Erica. M.S. den, World Wide Web. Thesis, Wake Forest University, Winston-Salem, North Carolina, U.S.A. BS 55 493

Nixon, K.C. & Crepet, W.L. 1993. Late Cretaceous fossil Scotese, C. 2000. PALEOMAP project. flowers of ericalean affinity. Amer. J. Bot. 80: 616-623. http://www.scotese.com/ Page, R.D.M. 1993. COMPONENT: Tree comparison soft Stevens, P.F., Luteyn,J.L., Oliver, E.G.H., Bell, T.L., Brown, ware for Microsoft Windows, version 2.0. The Natural E.A., Crowden, R.K., George, A.S., Jordan, G.J., Ladd, R., History Museum, London. Lemson, K, McLean, C.B., Menadue, Y., Pate, J.S., Stace, Powell, E.A. & Kron, K.A. 2001. An analysis of the phyloge H.M. & Weiller, C.M. 2004. Ericaceae In: Kubitski, K. netic relationships in the wintergreen group (Diplycosia, (ed.), The Families and Genera of Vascular Plants, Vol. 6. Gaultheria, Pernettya, Tepuia; Ericaceae). Syst. Bot. 26: Springer-Verlag, Berlin. Pp. 145-194. 808-817. Tiffney, B.H. 1985a. Perspectives on the origin of the floris Powell, E.A. & Kron, K.A. 2003. Molecular systematics of tic similarity between eastern Asia and eastern North the northern Andean blueberries (Vaccinieae, Vaccin- America./. Arnold Arbor. 66: 73-94. ioideae, Ericaceae). Int.J. Pl. Sei. 164: 987-995. Tiffney, B.H. 1985b. The Eocene North Atlantic land Raven, P.H. & Axelrod, D.I. 1974. Angiosperm biogeogra bridge: its importance in Tertiary and modern phyto phy and past continental movements. Ann. Missouri Bot. geography of the northern hemisphere. J. Arnold Arbor. Gard. 61: 539-673. 66: 243-273. Ronquist, F. 1997. Dispersal-vicariance analysis: A new Wiens, JJ- 1998. The accuracy of methods for coding and approach to the quantification of historical biogeogra sampling higher-level taxa for phylogenetic analysis: A phy. Syst. Biol. 46: 195-203. simulation study. SyV. Biol. 47: 381-397. Scholtz, A. 1985. The palynology of the upper lacustrine Wolfe, J.A. 1975. Some aspects of plant geography of the sediments of the Arnot pipe, Banke, Namaqualand. Ann. northern hemisphere during the late Cretaceous and S. African Mus. 95: 1-109. Tertiary. Ann. Missouri Bot. Gard. 62: 264-279. 494 BS 55

Appendix 1. Classification of Ericaceae. Taxonomy of subfamilies, tribes, and genera follow Kron et al. (2002a); genera and species numbers follow Stevens et al. (in press) and E. Brown (pers. comm.).

ERICACEAE (incl. Empetraceae, Epacridaceae, Monotropaceae, Pyrolaceae, Vacciniaceae) 121/4084 Subfam. Enkianthoideae 1/16 Enkianthus 16, E Asia, (Japan, Taiwan), Himalayas, N Indochina Subfam. Monotropoideae 15/50 Tribe Pyroleae 4/38 (Chimaphilao, Boreal-N temperate, North America south to Panama and Hispaniola, Europe, Asia; Moneses 2, N temperate North America, N Europe; Orthilia 1, Circumboreal, south to Mexico, Guatemala; Pyrola 30, Cir- cumboreal-N temperate, south to Guatemala, Himalayas to E China, N Sumatra) Tribe Monotropeae 9/10 (Allotropa 1, Pacific United States and Canada (California to S British Columbia); Cheilotheca 2 NE India (Assam), W Maleysia (Malay Peninsula, Perak and Sumatra); Hemitomes 1, Pacific United States and Canada (California to S British Columbia); Hypopitys 1, North America south to Guatemala, Europe to Asia (Japan, Korea, C China), Himalayas; Monotropa 1, N temperate North America south to Colombia, E Asia (Japan, Korea, E China), Himalayas; Monotropastrum 1, E Asia (Japan, Korea, C-SW China), Himalayas, Sumatra; Monotropsis 1, SE United States; Pityopus 1, Pacific United States (California and Oregon); Pleuricospora 1, Pacific United States and Canada (S British Columbia) Tribe Pterosporeae 2/2 (Pterospora 1, W North America south to N Mexico, Great Lakes region; Sarcodes 1, Pacific United States (California and Oregon) south to N Mexico (Baja California) Subfam. Arbutoideae 4/81 Arbutus 10, Pacific North America to Mexico, Europe, N Africa, Middle East, Canary Isl.; Arctostaphylos (incl. Arctous, Xylococcus) 60, Circumboreal, esp. W North America, Mexico to Guatemala; Comarostaphylis 10, W United States (Cali fornia) to W Panama; Ornithostaphylos 1, United States (S California) to Mexico (N Baja California) Subfam. Cassiopoideae 1/12 Cassiope 12, Circumboreal, Pacific North America, japan, Himalayas (Kasmir to Yunnan) Subfam. Ericoideae 19/1780 Tribe Ericeae 3/863 (Calluna 1, Europe, Asia Minor; Daboecia 2, Ireland to Spain and Azores; Erica (incl. 32 “minor gen era”) 860 Europe, scattered N Africa and Middle East, esp. southern Africa, Madagascar) Tribe Empetreae 3/5 (Ceratiola 1, SE United States; Corema 2, E North America, SE Europe, Azores; Empetrum 2, N tem perate and arctic, S Andes, Falkland Isl., Tristan da Cunha) Tribe Bejarieae 3/23 (Bejaria 15, SE United States, Cuba, Mexico to Bolivia, east to Guyana; Bryanthus 1, E Siberia, Kam chatka, Japan; Ledothamnus 7, Guayana Highland (Venezuela)) Tribe Phyllodoceae 6/28 (Elliottia (incl. Cladothamnus, Tripetaleia) 4 SE United States, Pacific North America (Oregon to Alaska), Japan; Epigaea 3, E North America, E Asia (Japan to Taiwan), Asia Minor, Caucasas; Kalmia (incl. Leiophyllum, Loiseleuria) 11, Circumboreal, North America, Cuba; Kalmiopsis 1, W United States (Oregon); Phyllodoce/, Circumpolar, N temperate (esp. W United States); Rhodothamnus 2, European Alps, E Turkey) Tribe Rhodoreae 4/861 (Diplarche 2, E Himalayas, SW China; Menziesia 7, Japan and Sakhalin, W North America, E United States; Rhododendron (incl. Azalea, Ledum, Tsusiophyllum) 850, Temperate Northern Hemisphere, E-SE Asia, esp. Himalayas and Malesia, Philippines, south to Australia (Queensland), E North America, mts. Europe, few spp. Circum boreal; Therorhodion 2, NE Asia, NW North America (W Alaska) ) Subfam. Harrimanelloideae 1/2 Harrimanella 2, Circumboreal (interruptedly), North America, Greenland, N Scandinavia to W Russia, Kamchatka, N Japan Subfam. Styphelioideae 35/520 BS 55 495

Tribe Prionoteae 2/2 {Lebetanthus 1, Patagonia, Tierra del Fuego; Prionotes 1, Australia (Tasmania)) Tribe Archerieae 1/6 (Archen a 6, Australia (Tasmania), New Zealand) Tribe Oligarrheneae 2/2 (Needhamiella (incl. Needhamid) 1 SW Australia; Oligarrhena 1, SW Australia) Tribe Richeeae 3/65 (Dracophyllum 48, E Australia, Lord Howe Isl., New Caledonia, New Zealand; Richea 11, SE Aus tralia; Sphenotoma 6, W Australia; Epacris 50, Australia, New Zealand, New Caledonia; Lysinema 5, SW Australia; Rupicola 4, Australia (New South Wales); Woollsia 1, Australia (Queensland and New South Wales)) Tribe Cosmelieae 3/27 (Andersonia 22, SW Australia; Cosmelia 1, SW Western Australia; Sprengelia 4, Australia, New Zealand) Tribe Styphelieae 19/357 (Acrotriche 14, Australia; Androstoma 1, New Zealand; AstroZoma 28, Australia; Brachyloma 7, Aus tralia; Coleanthera 3, SW Australia; Conostephium (inch Conostephiopsis) 7, SW Australia; Croninia 1, SW Western Australia; Cyathodes 19, Australia (Tasmania); Cyathopsis 1, New Caledonia; Decatoca 1, Papua New Guinea; Leptecophylla 13, Aus tralia, New Zealand, Papua New Guinea, W Pacifica; Leucopogon 215, Australia, New Zealand, New Caledonia, SE Asia, W Pacifica; Lissanthe 6, Australia; Melichrus 4, Australia; Monotoca 11, Australia; Pentachondra 5, Australia, New Zealand; Planocarpa 3, Australia (Tasmania); Styphelia, 11 southern Australia; TrochocarpaQ, Malesia (Papua New Guinea, Borneo, Celebes), Australia) Subfam. Vaccinioideae 45/1593 Tribe Oxydendreae 1/1 (Oxydendrum 1 E United States) Tribe Lyonieae 4/77 (Agarista (inch Agauria) 30, SE United States, SE Brazil, scattered Africa and Madagascar; Craibio- dendron (incl. Nuihonia) 5, S China (Yunnan), NE India, Indochina; Lyonia 35, E United States, West Indies, Mexico, E Asia (Japan to Pakistan, S to Malay Peninsula); Pieris (incl. ArcZm’ca) 7, E-SE United States, Cuba, E Asia (arc from S Kamchatka to Nepal)) Tribe Andromedeae 2/2 (Andromeda 1, Boreal-N temperate in Northern Hemisphere, N Japan; Zenobia 1, SE United States) Tribe Gaultherieae 6/246 (Chamaedaphne 1, Circumboreal-N temperate, E Asia south to N Japan, E North America south along Atlantic Coast to South Carolina; Diplycosia (incl. Pernettyopsis) 100, Malesia; Eubotrys 2, E United States; Gaultheria (incl. Chiogenes, Pernettya) 130, Circum-Pacific in North and South Hemisphers, E North America, SE Brazil, Himalayas, New Zealand and Tasmania; Leucothoe 6, Japan, Indochina (Burma, N Vietnam), SW China (Yunnan and SE Tibet), Pacific NW United States (California and Oregon); Tepuia 7, Guayana Highland (Venezuela)) Tribe Vaccinieae 32/1267 (Anthopteropsis 1, C Panama; Anthopterus 11, Costa Rica to NE Peru; Cavendishia 130, S Mexico to Bolivia, east to NW Brazil; Ceratostema (incl. Periclesia) 35, S Colombia to N Peru, Guyana; Costera 9, W Malesia; Demos- thenesia 11, C Peru to N Bolivia; Didonica 4, E Costa Rica to C Panama; Dimorphanthera 87, Malesia, mostly New Guinea, Philippines, W Pacifica; Diogenesia 13, W Venezuela to N Bolivia; Disterigma (incl. Killipielld) 35, Guatemala to Bolivia, east to Guyana; Gaylussacia 50, E North America, Colombia to Paraguay, SE Brazil; Gonocalyx 10, West Indies, Costa Rica to N Colombia; Lateropora 3, E Costa Rica to W Panama; Macleania 40, S Mexico to Peru; Mycerinus 3, Guayana Highland (Venezuela); Notopora 5, Guayana Highland (Venezuela); Oreanthes 7, Ecuador to N Peru; Orthaea (incl. Empedoclesia, Lysiclesia) 53, C Mexico to Bolivia, east to Guyana, Trinidad; Paphia (incl. Agapetes p.p.) 16, Malesia, esp. Papua New Guinea, W Pacifica, Australia (Queensland); Pellegrinia 5, C Peru; Plutarchia 11, Colombia to N Ecuador; Polyclila 1, C Bolivia; Psammisia 80, Costa Rica to Bolivia, east to Guianas and Trinidad; Rusbya 1, N Bolivia; Satyria 25, S Mexico to N Bolivia, Guianas to NW Brazil; Semiramisia 5, Venezuela to N Peru; Siphonandra 3, C Peru to N Bolivia; Sphyrospermum 25, S Mexico to N Bolivia, Guianas, West Indies; Themistoclesia 30, Costa Rica to N Bolivia; Thibaudia (incl. Calopteryx) 70; Costa Rica to N Bolivia, Guianas, NW Brazil; Utleya 1, Costa Rica; Vaccinium (incl. Agajtetop.p., Oxycoccus, Symphysia) ca. 500, Circumpolar-N temperate, Europe, North America, Japan, Himalayas to E-SE Asia, Malesia) 496 BS 55

Appendix 2. List of species (for more details see Kron et al. 2002a) used in the DIVA and Fitch parsimony character opti mization of biogeographic areas in the Ericales. DIVA characters are 1 = Africa, 2 = Australia, 3 = N America, 4 = Asia, 5 = Europe; Fitch scoring for 4 areas is 0 = Africa, 1 = Australia, 2 = N America, 3 = Eurasia; Fitch scoring for 2 areas is 0 = Laura- sia, 1 = Gondwana.

ASpecies DIVA Fitch Fitch 12345 (4 areas) (2 areas) Actinidia chinensis Planchon 01030 3 0 Arbutus canariensis Duhamel 10000 0 1 Bejaria racemosa Mutis ex L. f. 00100 2 0 Calluna vulgaris (L.) Hull 00001 3 0 Cassiope mertensiana (Bong.) G. Don 00011 2/3 0 Ceratiola ericoides Michaux 00100 2 0 Chamaedaphne calyculata (L.) Moench 00100 2/3 0 Clethra alnifolia L. 00100 2 0 Clethra arborea Vent. 10000 0 1 Cosmelia rubra R. Br. 01000 1 1 Cyrilla racemiflora L. 00100 2 0 Diapensia lapponica L. 00101 2/3 0 Diospyros virginiana L. 00100 2 0 Dracophyllum longifolium (J. R. Forster) Roem. and Schultes 01000 1 1 Enkianthus carnpanulatus G. Nicholson 00010 3 0 Epacris impressa Labill. 01000 1 1 Gaultheria eriophylla (Pers.) Sleumer 00010 3 0 Pentachondra pumila (Forster and G. Forster) R. Br. 01000 1 1 Promotes cerinthoides (Labill.) R. Br. 01000 1 1 Pyrola rotundifolia L. 00111 2/3 0 Rhododendron hippophaeoides Balf. f. and Forrest 00010 3 0 Symplocos paniculata Miq. 00100 2 0 Vaccinium macrocarpon Alton 00100 2 0 BS 55 497

Appendix 3. List of species (for more details see Kron et al. 2002a) used in the DIVA and Fitch parsimony character opti mization of biogeographic areas in Ericaceae. DIVA characters are 1 = Africa, 2 = South America, 3 = Australia, 4 = North America, 5 = Asia, 6 = Europe; Fitch scorings for 6 areas are: 0 = Africa, 1 = South America, 2 = Australia, 3 = North Amer ica, 4 = Asia, 5 = Europe; Fitch scorings for 2 areas are: 0 = Laurasia, 1 = Gondwana.

Species Subfamily 123456 6 areas 2 areas Agarista populifolia (Lam.) Judd Vaccinioideae 000100 3 0 Agarista salicifolia (Comm, ex Lam.) G. Don Vaccinioideae 100000 1 1 Andromeda polifolia L. Vaccinioideae 000101 3/5 0 Arbutus canariensis Duhamel Arbutoideae 100000 0 1 Arctostaphylos uva-ursi (L.) Sprengel Arbutoideae 000100 3 0 Bejaria racemosa Vent. Ericoideae 000100 3 0 Bryanthus gmelini D. Don Ericoideae 000010 4 0 Calluna vulgaris (L.) Hull Ericoideae 000001 5 0 Cassiope mertensiana (Bong.) G. Don Cassiopoideae 000111 3 4 5 0 Ceratiola ericoides Michaux Ericoideae 000100 3 0 Chamaedaphne calyculata (L.) Moench Vaccinioideae 000111 3 1 5 0 Chimaphila umbellata (L.) Barton Pyroloideae 000111 3/4/5 0 Corema conradi Torrey ex Loud. Ericoideae 000101 3/5 0 Craibiodendron yunnanenseW. Smith Vaccinioideae 000010 4 0 Daboecia cantabrica (Hudson) K. Koch Ericoideae 000001 5 0 Diplarche multiflora Hook. f. and Thomson Ericoideae 000010 4 0 Diplycosia acuminata Becc. Vaccinioideae 000010 4 0 Dracophyllum longifolium (J. R. Forster) Roem. and Schultes Styphelioideae 001000 2 1 Elliottia bracteata (Maxim.) Hook. F. Ericoideae 000100 3 0 Enkianthus campanulatus G. Nicholson Enkianthiodeae 000010 4 0 Epacris impressa Labill. Styphelioideae 001000 2 1 Epigaea repens L. Ericoideae 000100 3 0 Erica sicula Guss. Ericoideae 000010 4 0 Erica spiculifolia Salisb. Ericoideae 000010 4 0 Erica tetralix L. Ericoideae 000001 4 0 Eubotrys racemosa L. Vaccinioideae 000100 3 0 Gaultheria miqueliana Takeda Vaccinioideae 000010 4 0 Gaultheria shallon Pursh Vaccinioideae 000100 3 0 Harrimanella hypnoides Cov. Harrimanelloideae 000111 3/4/5 0 Kalmia angustifolia L. Ericoideae 000100 3 0 Kalmia buxifolia (Berg) Gift, Kron and Stevens Ericoideae 000100 3 0 Kalmia procumbens (L.) Gift, Kron and Stevens Ericoideae 000111 3/4/5 0 498 BS 55

Species Subfamily 123456 6 areas 2 areas Kalmiopsis leachiana (Henderson) Rehder Ericoideae 000100 3 0 Lebetanthus myrsinites Mach Styphelioideae 010000 1 1 Ledothamnus guyanensis Meissner Ericoideae 010000 1 1 Leucothoefontanesiana (Steudel) Sleumer Vaccinioideae 000100 3 0 Lyonia ferruginea (Walter) Nutt. Vaccinioideae 000100 3 0 Lyonia lucida (Lam.) K. Koch Vaccinioideae 000100 3 0 Menziesia pilosa Pers. Ericoideae 000100 3 0 Orthilia secunda (L.) House Monotropoideae 000111 3/4/5 0 Oxydendrum arboreum (L.) DC. Vaccinioideae 000100 3 0 Pentachondra pumila (Forster and G. Forster) R. Br. Styphelioideae 001000 2 1 Pernettya tasmanica Hook. f. Vaccinioideae 001000 2 1 Phyllodoce caerulea Bab. Ericoideae 000111 3/4/5 0 Phyllodoce empetriformis D. Don Ericoideae 000110 3/4 0 Pieris nana (Maxim.) Makino Vaccinioideae 000010 4 0 Pierisphillyraeifolia (Hook.) DC. Vaccinioideae 000010 3 0 Prionotes cerinthoides (Labill.) R. Br. Styphelioideae 001000 2 1 Pyrola rotundifolia L. Monotropoideae 000111 3/4/5 0 Rhododendron kaempferi Planchon Ericoideae 000010 4 0 Rhododendron tsusiophyllum Sugim. Ericoideae 000010 4 0 Rhodothamnus chamaecistus Rchb. Ericoideae 000001 5 0 Satyria warszewiczii Klotzsch Vaccinioideae 010000 1 1 Sprengelia incarnata W. Smith Styphelioideae 001000 2 1 Tepuia cardonaeX. C. Smith Vaccinioideae 010000 1 1 Therorhodion camtschaticum (Pallas) Small Ericoideae 000110 3/4 0 Fhcczmwm macrocarpon Aiton Vaccinioideae 000100 3 0 Vacanium méridionale Sw. Vaccinioideae 010000 1 1 Zenobia pulverulenta (Bartram) Pollard Vaccinioideae 000100 3 0 BS 55 499

Appendix 4. List of species used in the DIVA analysis of the Andean clade of the Vaccinieae (see Powell and Kron in press). DIVA characters are: 1 = Central America, 2 = Chocô, 3 = Andean Highlands Arc, 4 = eastern Lowland Arc, 5 = Antilles.

Species 1 2 3 4 5 Anthopterus wardii Ball 1 1 0 0 0 Cavendishia bracteata (Ruiz and Pav. Ex J. St.-Hil.) Hoer. 1 0 1 0 0 Cavendishia capitulataj. D. Smith 1 0 1 0 0 Cavendishia complectens Hemsl. 1 0 1 0 0 Cavendishia grandifolia Hoer. 0 0 1 0 0 Cavendishia martii (Meissner) A. C. Smith 0 0 1 0 0 Ceratostema lanigerum (Sleumer) Luteyn 0 0 1 0 0 Ceratostema rauhii Luteyn 0 0 1 0 0 Ceratostema reginaldii (Sleumer) A. C. Smith 0 0 1 0 0 Ceratostema silvicolaA. C. Smith 0 0 1 0 0 Demosthenesia pearcii (Britton) A. C. Smith 0 0 1 0 0 Diogenesia racemosa (Britton) Sleumer 1 0 1 0 0 Disterigma alatemoides (Kunth in H.B.K.) Niedenzu 0 0 1 0 0 Disterigma ovatum (Rusby) S. F. Blake 0 0 1 0 0 Disterigma pernettyoides (Wedd.) Niedenzu 0 0 1 0 0 Disterigma rimbachii (A. C. Smith) Luteyn 1 0 0 0 0 Disterigma trimerum Wilbur and Luteyn 0 0 1 0 0 Macleania bullata Yeo 0 0 1 0 0 Madeania coccoloboides A. C. Smith 0 0 1 0 0 Macleania cordifolia Benth. 0 0 1 0 0 Macleania insignis M. Martens and Galeotti I 0 0 0 0 Polyclita turbinata A. C. Smith 0 0 1 0 0 Psammisia dolichopoda A. C. Smith 1 1 1 0 0 Psammisia ecuadorensis Hoer. 0 0 1 0 0 Psammisia sodiroi Hoer. 0 0 1 0 0 Psammisia ulbrichiana Hoer. 1 0 1 0 0 Satryia vargasii A. C. Smith 0 0 1 0 0 Satyria allenii A. C. Smith 1 0 0 0 0 Satyria boliviana Luteyn 0 0 1 0 0 Satyria cerander (Dunal) A. C. Smith 0 0 0 1 0 Satyria grandfolia Hoer. 0 1 1 0 0 Satyria leucostoma Sleumer 0 0 1 0 0 Satyria meianthaj. D. Smith 1 0 0 0 0 Satyria polyantha A. C. Smith 0 0 1 0 0 Satyria sp. nov. 1 0 0 0 0 500 BS 55

Species 1 2 3 4 5 Satyria ventricosa Luteyn 1 0 0 0 0 Satyria warszewiczii Klotzsch 1 0 0 0 0 Semiramisia speciosa (Benth.) Klotzsch 0 0 1 0 0 Sphyrospermum ellipticum Sleumer 1 0 1 0 0 Symphysia racemosa (Vahl) Stearn 0 0 0 0 1 Themistoclesia costaricensis Luteyn and Wilbur 0 0 1 0 0 Themistoclesia epiphytica A. C. Smith 0 0 1 0 0 Thibaudia costaricensis Hoer. 1 0 0 0 0 Thibaudia densiflora (Herzog) A. C. Smith 0 0 1 0 0 Thibaudia diphylla Dunal 0 0 1 0 0 Thibaudia floribunda Kunth in H. B. K. 0 0 1 0 0 Thibaudia inflata Luteyn 0 0 1 0 0 Thibaudia litensis Luteyn 0 0 1 0 0 Thibaudia macrocalyx Remy 0 0 1 0 0 Thibaudia martiniana A. C. Smith 0 0 1 0 0 Thibaudia pachyantha A. C. Smith 0 0 1 0 0 Thibaudia parvifolia (Benth.) Hoer. 0 0 1 0 0 Thibaudia tomentosa Hoer. 0 0 1 0 0 Vaccinium poasanumj. D. Smith 1 0 0 0 0